MARINE ECOLOGY PROGRESS SERIES Vol. 38: 37-44. 1987 - Published May 21 l Mar. Ecol. Prog. Ser. l

Partial predation on tropical gorgonians by Cyphoma gibbosum (Gastropoda)

C. Drew ~arvell'& Thomas H. suchanek2

' Section of Ecology and Systematics, Cornell University, Ithaca, New York 14853,USA Division of Environmental Studies, University of California, Davis, California 95616, USA and Bodega Marine Laboratory, PO Box 247, Bodega Bay, California 94923, USA

ABSTRACT: Cyphoma gibbosum (Gastropoda, Ovulidae), a generalized predator on tropical gorgo- nians, forages selectively among gorgonian on shallow reefs at St. Croix, U.S. Virgin Islands. Mean residence times of marked snails on prey taxa ranged from 1.8 d on Eunicea spp. to 4.7 and 10 d on Gorgonia ventalina and Plexaurella dichotoma respectively. Juveniles were sedentary and remained on single hosts throughout the study period. An analysis of wounds caused by C. gibbosum on gorgonians revealed that colonies of some taxa were consistently stripped of tissue, baring the underlying proteinaceous axis, while others were only superficially grazed. Wounds baring the axial skeleton were considerably more severe than superficial wounds because the bared skeleton could be colonized by algae causing subsequent tissue regeneration to be inhibited. Within all species, wounds were not restricted to any single portion of the colony. However, most wounds occurred within the central regions of colonies and the lowest portions of colonies were seldom damaged. The short residence times and superficial grazing on some taxa such as Eunicea spp. and Muncea spp. may be a consequence of heavy spicular armor over polyps and over the proteinaceous axis in those taxa. Deep wounds to the axial skeleton occurred only on taxa with smaller spicules and a smaller proportion of spicules in the coenenchyme by dry weight. Residence time on a prey species was inversely pro- portional to both maxlmum spicule length and percent composition of spicules. Short residence times and shallow wounds on colonies of heady splculed species may be a response by C. gibbosum to foraging on suboptimal, heavlly defended resources Despite the short residence times, these potentially suboptimal prey taxa were regularly visited and preyed upon. This suggests that factors other than spicular architecture, such as gorgonian chemistry, may also play a role in the foraging of C. gibbosum.

INTRODUCTION Palumbi 1979, Jackson 1983, Harvell 1984a, 1985). Understanding the interactions of partial predators Rather than killing their hosts and prey, many con- with their prey is particularly important in tropical sumers such as herbivores, parasites, and grazers on reef habitats where benthic communities are often colonies routinely remove only small quantities of dominated by reef-building colonial (Jackson tissue (Price 1980, Lubchenco & Gaines 1981, Thomp- 1983). son 1982, Harvell1984a, 1986). Partial predation (sensu Although scleractinian and gorgonian corals (Cary Jackson & Palumbi 1979, Hawell 1984a) is of particular 1918) dominate many benthic communities in the theoretical interest because natural selection will oper- tropics, and gorgonian corals are known to be heavily ate differently on prey populations in which individuals invested with biologically active toxins (Collet al. 1982, typically survive encounters with predators. Attacks by Fenical 1982, Gerhart 1983, 1984, Bakus et al. 1986), non-lethal predators should favor inducible defenses little is known of the patterns of attack by pafial and defenses that limit area1 extent of damage (Harvell predators, or the consequences of attack and subse- 1984a, b, 1986, Rhoades 1985). Colonial invertebrates quent colony recovery. Types of attacks by corallivores are only rarely killed by their predators and, due to are diverse and include tissue stripping (Birkeland & their modular body plan and capacity for regeneration, Gregory 1975, Brawley & Adey 1982, Glynn & Welling- may be little impaired by consumer attacks (Jackson & ton 1983, Wahle 1985), nipping of branch tips (Glynn et

O Inter-Research/Printed in F. R. Germany Mar. Ecol. Prog. Ser. 38:3744, 1987

al. 1972, Neudecker 1979, Wellington 1982, Glynn & METHODS AND RESULTS Wellington 1983, Wahle 1985), and removal of indi- vidual polyps (Birkeland & Neudecker 1981, Brawley & Study sites Adey 1982, Lasker 1985). Most corals appear to recover readily from removal of individual polyps and damage All experimental work was conducted in St. Croix, to branch tips (Neudecker 1979, Wellington 1982, U.S. Virgin Islands, during NULS-1 HYDROLAB mls- Wahle 1983a), but even minor amounts of tissue strip- sion 82-12 from 26 August to 21 September 1982. (See ping can be catastrophic because fast-growing algae or Suchanek 1983 for location map.) A shallow (4 to 10 m) Millepora spp. (Wahle 1980) can permanently colonize site was located on the gorgonian-dominated forereef bared skeleton and prevent subsequent tissue regener- with western exposure. The study site adjoined the ation (Wahle 1983a, 1985, Harvell & Suchanek pers. deeper HYDROLAB site at Salt River Canyon. Samples obs.). for spicule analysis were collected in the forereef at The effects of partial predation can be quantified as Mama Rhoda Reef at Chub Cay in the northwestern the proportion of an individual colony killed, but the Bahamas (25" 21' N, 77" 52' W). functional role of lost units must also be considered since all parts of a colony do not function equivalently Feeding selectivity (Palumbi & Jackson 1983, Harvell 1984a). Most col- onies have ontogenetically based funcbonal gradients; Methods. Prey selection and residence times were thus the consequences of an attack depend on its quantified by marking all Cyphoma gibbosum and location and magnitude. For example, in some bryo- occupied gorgonians in the study area (100 m2) in St. zoans, the central, oldest regions of a colony often Croix and recensusing the location of each snail daily. cannot regenerate as rapidly as the outer perimeter Each snail was uniquely marked by a system of 2 (Palumbi & Jackson 1983, Harvell 1984a). Attacks to notches filed on the shell that coded for individuals the center of the colony may more often prevent colony from 1 to 80. This was a minimally disruptive technique recovery than attacks to the edge. Thus the conse- for marking large numbers of snails in situ: specimens quences of damage to a colony are determined by both were handled only briefly, and their appearance was the location and scale of damage. generally unchanged. The behavior of marked indi- In this paper, we report on the interaction between a viduals did not differ noticeably from the behavior of 5 tissue-stripping tropical corahvore, Cyphoma gibbo- individuals with natural distinctive marks that we mon- sum (Molluscs, Gastropoda) and its upright gorgonian itored for the duration of the study (12 d). prey. Although C. gibbosum feed exclusively on gorgo- The proportion of prey available was determined by nian corals, they can be considered trophic generalists recording the identity of every colony within the study because most available species in several gorgonian area. Because it was impossible to reliably identify all families are included in their diet (Birkeland & Gregory the gorgonian species in the field, we lumped species 1975). C. gibbosum are ubiquitous throughout the into taxonomic and functional groups where necessary. Caribbean on shallow gorgonian-dominated reefs (Kin- We combined flexuosa, P. homomalla, and zie 1971, 1974, Birkeland & Gregory 1975, Gerhart Pseudoplexaura crucis into a Plexa ura group, and 1986). Two striking aspects of the interaction between lumped Muricea spp., Eunicea mammosa, and Eunicea C. gibbosum and its gorgonian prey are (1) the small spp. into a Eunicea group. The remaining genera and amount of damage and low probabihty of mortality some species could be reliably distinguished on the suffered by each attacked colony and (2) the great basis of field characters. mobility of C. gibbosum while foraging among colonies A predator is considered to feed selectively when it (Birkeland & Gregory 1975, Gerhart 1986). This is a takes any prey item in disproporbonate numbers rela- common pattern for many predators attaclung colonial tive to its availability. A number of 'electivity indices' invertebrates (Harvell pers. obs.) and may be, in part, a exist to analyze the discrepancy between the pro- consequence of colony defenses (Gerhart 1986). The C. portion of prey available and the proportion of prey gibbosum-gorgonian interaction is a tractable system attacked. A critical problem in the interpretation of for analyzing intra- and inter-colony patterns of preda- some of these analyses is the way relatlve abundance tor attack and colony defenses. We address the follow- affects the magnitude of the electivity index. For exam- ing 3 questions: (1) What are the intra-colony patterns ple, the Ivlev index weights electivities for rare prey of damage inflicted by C. gibbosum on the most heavily disproportionately by dividing the difference between attacked taxa of gorgonians; (2)Do patterns of damage available and selected prey by the sum of the two. reflect underlying variations in colony function or mor- Because there is considerable variation in the behavior phology; and (3) What are the interspecific patterns of of different electivity indices, we applied 3 of the most attack? widely used indices to the data: Ivlev's E (1961), Harvell & Suchanek: Gastropod predation on tropical gorgonians

Table 1. Cyphoma gibbosum. Comparison of different electivity indices calculated for snails foraging on gorgonlans at St. Croix

Taxon Proportion Proportion Chesson's Ivlev's Jacobs' available eaten ci E Log Q (N= 365) (N= 149)

Plexaurella dichotorna 0.05 0.07 0.27 0.22 0.15 Eunicea group 0.19 0.23 0.24 (0.01)' 0.09 0.10 Plexaura group 0.62 0.66 0.21 (0.01)' 0.03 0.07 Briareurn asbestinurn 0.01 0.01 0.19 (0.02)' 0 0 Pseudopterogorgia americanum 0.07 0.02 0.05 (0.15)' -0.55 -0.57 Gorgonia ventalina 0.05 0.01 0.03 (0.81)' -0.70 -0.87

' Data recalculated from Birkeland & Gregory (1975)

Chesson's cr (1978), and Jacobs' log Q (1974). These Another measure of selectivity for a colony is resi- were all developed for motile predators feeding on dence time, which can vary independently of electivity. motile prey, but the extension to sessile prey does not Residence times of adult Cyphoma gibbosum (Table 2) violate any underlying assumptions. Electivity indices varied significantly among different prey groups (Plex- were calculated from the proportion of prey selected aura, Eunicea, and Plexaurella) (Kruskall Wallis Test, and the proporhon of prey available. The proporbon of x2= 8.712, p < 0.013) where observations were numer- prey selected was calculated by dividing the number of ous enough to permit analysis. A Median Test (Zar times a prey taxon was chosen by the total number of 1974) showed that residence time was significantly choices made. longer on the Plexaura group than on the Eunicea To determine if Cyphoma gibbosum varied the dura- group (x2= 7.95, p < 0.005). Increased sample sizes for tion of attacks on colonies of different species, we rarer taxa, such as Pseudopterogorgia spp. and Gor- measured residence time: the number of days a snail gonia ventalina, would probably yield significantly remained on a prey colony. Residence times were only longer residence times than for other taxa. Juvenile C. analyzed when the entire tenure of a snail on a colony gibbosum do not move frequently among prey species; was observed; individuals that stayed the entire study all juveniles remained on single hosts for the entire period on a single colony were assigned a residence sample period (Table 2). time of 12 d for comparative analyses. Thus residence times in excess of 12 d will be underestimated by our observations. We monitored over 80 snails intensively Scar length, depth, and position to improve our estimates of residence time on the most abundant taxa. Methods. For each of 6 taxa, Plexaurella dichotoma, Results. Table 1 summarizes the indices obtained the Plexaura group (P. homomalla, Plexaura spp., P. using 3 different measures of electivity. There are 2 flexuosa, and Pseudoplexaura crucis), the Eunicea important features of this companson to note: (1) the group, Pseudopterogorgia americanum, Pseudoptero- order (or 'preference' for the different prey items) does gorgia spp. (P, ngida and P, acerosa), Gorgonia ventali- not change with different indices, giving us confidence in the relative ranking of preference for prey, (2) the Table 2. Cyphorna gibbosum. Summary table of electivity and range of values varies with the index used. Therefore, residence times (d) on different taxa of gorgonians the rank order of preferences is relatively robust, while the absolute magnitude of scores for preferences is not. Taxon Electivity Residence time (d) 'U' For our purposes, the index (Chesson 1978) was (Chessons's a) Mean SD (N) most useful because (1) it varies continuously between 0 and 1 and is thus 'bounded' and (2) relative prey Plexaurella dichotorna 0.27 1.8 1.2 (6) abundance affects the magnitude of the index so that Eunicea group 0.24 1.4 0.9 (29) selection of rare prey is detected, but the electivity for Plexaura group 0.21 2.9 2.4 (50) rare prey is not disproportionate. Our analysis failed to Briareum asbestinurn 0.19 1.0 0 (2) Pseudopterogorgia 0.05 4.7 4.1 (3) reject the null hypothesis that Cyphorna gibbosum american um attacked colonies in proportion to their relative abun- Gorgonia ventalina 0.03 10.0 0 (2) dance (x2,p > 0.05) (Table 1); therefore, we conclude All adults 3.3 3.4 (92) that there is no active selection of prey colonies during Juvenile C. gibbosurn 12.0 0 (9) the initial encounter phase of interactions. 4 0 Mar. Ecol. Prog. Ser. 38: 37-44, 1987

Fig. 1, (a) Cyphorna gibbosum feeding on Briareum asbestinum and causing only superficial dam- age. (b) C. gibbosum feeding on the gorgonian Plexaura spp. The deep feeding scar has exposed the underlying gorgonin skeleton na, and Briareum asbestinum, we measured the length Intra-colony locations of scars were examined to of naturally occurring feeding scars (usually with a detect consistent locations of preferred attack. The snail still present), the distance from the base of a height from colony base to scar initiation was divided colony to the base of a scar (here defined as the point of by the total height of a colony to provide a normalized initiation), and the total height of each colony. measure for comparison among species. We scored the depth of naturally occurring feeding Results. Feeding scars were distributed throughout scars as either superficial or skeletal. Skeletal wounds the middle regions of colonies on all species. In Fig. 2 completely bared the underlying gorgonin skeleton we have plotted the point of scar initiation normalized (Fig. 1). These categones were straightforward to dis- by colony height. The 95 % confidence intervals tinguish and are functionally significant to the colony. around the means are large. Scars were usually not For scars on Briareum asbestinum, a scleraxonian with- initiated in the lower 20 O/O of colonies, suggesting that out a gorgonin skeleton, we classified skeletal wounds basal regions are avoided. With the exception of Plex- as those that exposed the innermost spicular layer. The aurella dichotoma, on which feeding scars were initi- frequency of individuals with skeletal scars in each ated in a narrow band in the midsection of colonies, taxon was compared over all taxa with a G-Test (Sokal scars appeared to be initiated broadly throughout cen- & Rohlf 1981). tral regions of colonies. Harvell & Suchanek. Gastropod predation on tropical gorgonians

ing Plexaurella dichotoma, Briareum asbestinum, and the Eunicea group. Frequencies of skeletal wounding are not significantly different within each of the groups (G-Test, p > 0.05), but are significantly different among groups (G-Test, p < 0.001).

Spicule size and composition

Methods. Spicule size and percent composition in gorgonian colonies were analyzed to determine if max- imum spicule size and percent composition of spicules were correlated with short residence times and super- ficial wounding. Spicule size was reported as the max- imum spicule length given in Bayer (1961). The pro- portion of spicules was determined as the ash-free dry weight/total dry weight. Sections of gorgonian col- onies, 3% cm long, were collected at Chub Cay in the Bahamas and immediately preserved in 4 % buffered formalin. Samples were soaked for l h in dishlled water, the central gorgonin core removed, and the GORGONIAN TAXA outer tissue dried at 60°C in a drying oven. After Fig. 2. Mean height of initlahon of scars normalized by colony colonies were completely dry (1 d after they stopped height (mean and 95 % confidence intervals) on 6 taxa of losing weight), they were weighed and placed in a gorgonians. Abbrev~ations for taxa are as follows: Pseudo: muffle furnace at 450°C for 4 h. For thls interval and Pseudopterogorgia americanum; Gorgonia: Corgonia ven- tahna; Plexaura: Plexaura group; Briareum: Briareum asbes- temperature, only organic material should be com- hnum; Plexaurella: Plexaurella dichotoma; Eunicea: Eunicea busted, and spicules should remain intact (Paine 1964). group Above 50OoC, water of hydration may be separated from the calcium carbonate causing a further, con- Scar lengths did not vary significantly among prey founding loss of weight (Paine 1964, Harvell pers. obs.). species (Table 3) and were not correlated with colony To be certain that calcium carbonate did not lose height (Pearson Product Moment correlation coefficient weight during this procedure, inorganic reagent-grade p > 0.05 for all taxa). calcium carbonate was also processed with the gorgo- Scar depth varied significantly among prey taxa (G = nian samples; there was no significant weight loss in 5 56.34, p<0.001; Table 3). Gorgonian taxa could be replicate samples processed. divided into 3 groups based upon the depth of wounds: Results. The dry weight composition of spicules var- (1) those that were usually (>go%) wounded to the ied significantly among taxa, ranging from approxl- axis, including Pseudopterogorgia spp. and P. amen- mately 35 % for Pseudopterogorgia americanum to canum; (2)those that were often (50 to 75 %) wounded approximately 85 O/O for Muncea spp. (Fig. 3). Four taxa to the axis, including Gorgonia ventahna, the Plexaura stand out as having the highest percent composition of group, and Plexaura flexuosa; and (3) those that were spicules: the Eunicea group, Plexaurella dichotoma, rarely or never (0 to 15 %) wounded to the axis, includ- Plexaura flexuosa, and Muricea spp.

Table 3. Length (cm) and depth of wounds caused by Cyphoma gibbosum on gorgonians. Wound depths were classified as skeletal or non-skeletal. Scar depth is reported as the percentage of skeletal wounds. -: no sample

Taxon Scar length Scar depth Mean SD (NI YO (N)

Plexa urella dichotoma 7.2 6.8 (5) 0 (9) Eunlcea group 15.0 8.8 (9) 6 (17) Bnareum asbestinum 13.4 7.7 (7) 14 (8) Plexaura flexuosa 11.9 10.5 (9) 62 (8) Gorgonia ventafina 5 0 (6) Plexaura group 12.0 7.9 (21) 66 (7) Pseudop terogorgia amencan urn 11.7 8.1 (10) 95 (20) Pseudop terogorgia spp. - 100 (10) 42 Mar. Ecol. Prog. Ser. 38: 37-44, 1987

Maximum spicule length varied among taxa (Fig. 4) DISCUSSION and with the exception of Plexaurella dchotoma, which has very small spicules, was generally pro- The extent of damage by Cyphoma gibbosum to portional to percent composition of spicules (Pearson gorgonian colonies varied among prey taxa. Only one correlation coefficient 0.60, N = 7) (Fig. 4). species was consistently wounded to the skeleton (Pseudopterogorg'a amencan um), exposing it to inva- sion by colonizing algae. The depth of attack on gorgo- nian colonies appears to be determined by spicule size and architectural differences among prey taxa. Large spicules embedded in soft tissue or a high percent composition of spicules may act as a barrier to tissue- stripping predators such as C. gibbosum. Thus taxa with small or a low composition of spicules may routinely suffer attacks from which recovery is inhi- bited. In addition to the depth of the wound, the configura- tion of tissue loss also has major consequences for colony function. For example, in bryozoans, Harvell (1985) has shown that grazing by molluscs can acceler- ate reproduction of the entire colony. Wahle (1983b) has demonstrated that 'grdling' a colony of Plexaura hornomalla can isolate and desynchronize the repro- ductive function of upper branches. Most attacks of Cyphoma gibbosum leave vertical scars not exceeding 1 cm in width (pers. obs.) and not girdling branches; thus branch tips are only occasionally isolated by C. GORGONIAN TAXA gibbosum attacks. Within colonies, attacks were initi- Fig. 3. Spicule composition of predominant prey taxa. Mean ated predominantly in the middle and thus were less (N = 4) and 95 % confidence intervals are plotted. Taxonomic frequent on the lower 20 % of colonies. The attack zone abbreviahons as in Fig. 2, plus P. homorn.: Plexaura was broad enough on most taxa to suggest that there homomalla; P. flex.: Plexaura flexuosa; Muricea: Muricea spp. were no localized preferred sites within colonies. Interspecific differences in prey quality appear to determine residence times of Cyphoma gibbosum, as well as the extent of damage to colonies. C. gibbosum spend significantly less time on heavily spiculed taxa such as Muricea spp., Eunicea spp., and Plexaurella dichotoma than on taxa from which they can extract more tissue (r = -0.49 [residence time with % compo- sition], r = -0.63 [residence time with spicule length]; N = 7). Thus, in addition to playing a role in colony architecture and support, spicules may also function as a defense against predators. The observed distribution of Cyphoma gibbosum on gorgonians results from the interaction of both initial electivity and residence time. For comparison, we have recalculated Birkeland & Gregory's data (1975) on elec- tivity of foraging C. gibbosum for different gorgonian species (Table 1). They calculated electivity from cen- suses of C. gibbosum on marked gorgonians; thus their measure of electivity combines both the choices made by C. gibbosum among prey and the residence time on GORGONIAN TAXA different prey. Their data show marked preference of C. gibbosum for Gorgonia ventalina, in complete con- Fig. 4. Maximum spicule lengths of predominant prey taxa (lengths taken from Bayer 1961). Taxonomic abbreviations as trast to our result of no significant electivity for any in Fig. 2 & 3 species. Because we followed the foraging choices of Harvell & Suchanek: Gastropod predation on tropical gorgonians 43

marked individuals, we were able to separate electivity lated that while a population of Cyphoma gibbosurn from residence time. We found that while electivity for may account for 62 O/O of annual tissue loss to a popula- G. ventalina was not greater than that for other species, tion of gorgonians, they caused only 4 O~Oof the mortal- residence times were longest on G. ventalina. Thus it ity. However, partial consumers may have dramatic appears that C. gibbosuin can attack prey in proportion sublethal effects on morphology and patterns of alloca- to their relative abundance, yet shll exercise selection tion to growth, reproduction, and defense within among prey species by varying residence time. We attacked colonies (Kaufman 1981, Wahle 1983b, 1986, predict that the foraging behavior of any partial preda- Harvell 1984a, b, 1985, 1986). For example, one species tor can be divided into these 2 components, and that of temperate bryozoan produces defensive spines residence time may often be the more important vari- (Yoshioka 1982, Harvell 1984a) and initiates reproduc- able in determining the observed patterns of prey tion (Harvell 1985) in response to attacks by partial selection. predators. These temporally varying responses to pre- Diet mixing has been invoked as an explanation for dation may in turn decrease the quality of the prey and the generalized foraging tendencies of several preda- encourage consumers to reduce the duration of attacks. tory and herbivorous partial predators. Birkeland & The short duration of most attacks by C. gibbosum Gregory (1975), who also noted frequent movements of could be a consequence of inducible structural or individual Cyphoma gibbosum among gorgonian prey chemical defenses (Harvell 1984a, Gerhart 1986). Thus species, concluded that C. gibbosum move often as in plants (Rhoades 1985), many colonies may have among prey to fulfil1 a diet-mixing requirement. Other complex combinations of constitutive and inducible corallivores also diet mix and maintain a wider diet defenses which govern the foraging behaviors of their breadth than expected from prey abundance alone. consumers. Birkeland & Neudecker (1981) demonstrated diet mix- ing in the butterfly fish Chaetodon capistratus, which Acknowledgements. This research was supported in part by a feeds on a range of scleractinian and gorgonian corals. NATO postdoctoral fellowship to C.D.H., NSF OCE8516407 to Some herbivorous insects are known to forage widely C.D.H. and R. T. Paine, NSF OCE8400818 to R. R. Strathmann, and NOAA NA-82-AAA-00872 and 01344 grants to T.H.S. L. to detoxify an otherwise unpalatable diet (Scriber Madin generously provided laboratory space for C.D.H. on a 1984). There are several mechanisms by which the cruise to Chub Cay and at Woods Hole Oceanographic Insti- detoxification hypothesis may act: (1) compounds may tute. We are particularly grateful to M. Colgan for cheerfully interact so that combining feeding deterrents from participating in long hours underwater at St. Croix and to C. Greene for assishng with collections in the Bahamas. This different species may nullify the negative effects of manuscript benefited from comments by C. Greene, M. certain compounds; (2) consumers may have an abso- Dethier, R. Strathmann, and 4 anonymous reviewers. lute tolerance for parhcular compounds that limits resi- dence hme on any one species, but allows mixing of different compounds (Berenbaum 1986). While our LITERATURE CITED observations suggest that residence time is in part Bakus, G. J., Targett, N. M., Schulte, B. (1986). Chemical limited by spicule composition or architecture, the ini- ecology of marine organisms: an overview. J. chem. 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This arbcle was submitted to the editor; lt was accepted for printing on February 24, 1987